Certain secondary antiepileptic drugs can rescue hippocampal injury following a critical growth period despite poor anticonvulsant activity and cognitive deficits

Epilepsy and Behavior

Volumn 29, Issue 3, 2013, Pages 466-477

  Halbsgut, Lisa R ^c   Fahim, Eiris ^b   Kapoor, Karnika ^b   Hong, Henry ^b   Friedman, Linda K ^a,b,c  

^a NEW YORK MEDICAL COLLEGE   (United States)

^b NEW YORK INSTITUTE OF TECHNOLOGY   (United States)

^c SETON HALL UNIVERSITY   (United States)

Author keywords

Antiepileptic drugs; Cognition; Development; Hippocampus; Injury; Seizures

Indexed keywords

ANTICONVULSIVE AGENT; CARBAMAZEPINE; KAINIC ACID; LAMOTRIGINE; PHENYTOIN; TOPIRAMATE; VALPROIC ACID;

ADOLESCENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTICONVULSANT ACTIVITY; ARTICLE; BENIGN CHILDHOOD EPILEPSY; BRAIN INJURY; BRAIN PROTECTION; BRAIN REGION; COGNITIVE DEFECT; CONTROLLED STUDY; ELECTROENCEPHALOGRAPH; EPILEPTIC STATE; FEMALE; LATENT PERIOD; LEARNING; MALE; MAZE TEST; MEMORY; MEMORY DISORDER; NEUROPROTECTION; NONHUMAN; PERINATAL PERIOD; RAT; SEIZURE; SILVER IMPREGNATION;

ANTIEPILEPTIC DRUGS; COGNITION; DEVELOPMENT; HIPPOCAMPUS; INJURY; SEIZURES;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; ANTICONVULSANTS; BODY WEIGHT; BRAIN INJURIES; CELL COUNT; COGNITION DISORDERS; DISEASE MODELS, ANIMAL; EXCITATORY AMINO ACID AGONISTS; FEMALE; HIPPOCAMPUS; HUMANS; KAINIC ACID; MALE; MAZE LEARNING; RATS; RATS, SPRAGUE-DAWLEY; SEIZURES; TREATMENT OUTCOME;

EID: 84887821592     PISSN: 15255050     EISSN: 15255069     Source Type: Journal    
DOI: 10.1016/j.yebeh.2013.08.019     Document Type: Article

References (71)

1. Bergman I., Painter M.I., Hirsch R.P., Crumrine P.K., David R. Outcome of neonates with convulsions treated in an intensive care unit. Ann Neurol 1983, 14:642-647.
2. Hauser W.A., Kurland L.T. The epidemiology of epilepsy in Rochester, Minnesota, 1935 through 1967. Epilepsia 1975, 16:1-66.
3. Rowe J.C., Holmes G.L., Hafford J., Baboval D., Robinson S., Philipps A., et al. Prognostic value of the electroencephalogram in term and preterm infants following neonatal seizures. Electroencephalogr Clin Neurophysiol 1985, 60:183-196.
4. Brunquell P.J., Glennon C.M., DiMario F.J., Lerer T., Eisenfeld L. Prediction of outcome based on clinical seizure type in newborn infants. J Pediatr 2002, 140:707-712.
5. Scher M.S., Painter M.J., Bergman I., Barmada M.A., Brunberg J. EEG diagnoses of neonatal seizures: clinical correlations and outcome. Pediatr Neurol 1989, 5:17-24.
6. van Esch A., Ramlal I.R., van Steensel-Moll H.A., Steyerberg E.W. Outcome after febrile status epilepticus. Dev Med Child Neurol 1996, 38:19-24.
7. Eriksson K.J., Koivikko M.J. Status epilepticus in children: etiology, treatment, and outcome. Dev Med Child Neurol 1997, 39:652-658.
8. Bocti C., Robitaille Y., Diadori P., Lortie A., Mercier C., Bouthillier A., et al. The pathological basis of temporal lobe epilepsy in childhood. Neurology 2003, 60:191-195.
9. Shorvon S.D. Epidemiology, classification, natural history, and genetics of epilepsy. Lancet 1990, 336:93-96.
10. Liu Z., Gatt A., Werner S.J., Mikati M.A., Holmes G.L. Long-term behavioral deficits following pilocarpine seizures in immature rats. Epilepsy Res 1994, 19:191-204.
11. Cavalheiro E.A., Silva D.F., Turski W.A., Calderazzo-Filho L.S., Bortolotto Z.A., Turski L. The susceptibility of rats to pilocarpine-induced seizures is age-dependent. Brain Res 1987, 465:43-58.
12. Nabbout R., Vezzani A., Dulac O., Chiron C. Acute encephalopathy with inflammation-mediated status epilepticus. Lancet Neurology 2011, 10:99-108.
13. Ravizza T., Gagliardi B., Noe F., Boer K., Aronica E., Vezzani A. Innate and adaptive immunity during epileptogenesis and spontaneous seizures: evidence from experimental models of human temporal lobe epilepsy. Neurobiol Dis 2006, 29:142-160.
14. Jensen F.E., Holmes G.L., Lombroso C.T., Blume H.K., Firkusny I.R. Age-dependent changes in long-term seizures susceptibility and behavior after hypoxia in rats. Epilepsia 1992, 33:971-980.
15. Stafstrom C.E., Chronopoulos A., Thurber S., Thompson J.L., Holmes G.L. Age-dependent cognitive and behavioral deficits after kainic acid seizures. Epilepsia 1993, 34:420-432.
16. Stafstrom C.E., Thompson J.L., Holmes G.L. Kainic acid seizures in the developing brain: status epilepticus and spontaneous recurrent seizures. Brain Res Dev Brain Res 1992, 65:227-236.
17. Kim J.S., Kondratyev A., Tomita Y., Gale K. Neurodevelopmental impact of antiepileptic drugs and seizures in the immature brain. Epilepsia 2007, 48(Suppl. 5):19-26.
18. Kim J., Kondratyev A., Gale K. Antiepileptic drug-induced neuronal cell death in the immature brain: effects of carbamazepine, topiramate, and levetiracetam as monotherapy versus polytherapy. J Pharmacol Exp Ther 2007, 323:165-173.
19. Forcelli P.A., Kozlowski R., Snyder C., Kondratyev A., Gale K. Effects of neonatal antiepileptic drug exposure on cognitive, emotional, and motor function in adult rats. J Pharmacol Exp Ther 2012 Mar, 340:558-66.
20. Massa H., Lacoh C.M., Vutskits L. Effects of morphine on the differentiation and survival of developing pyramidal neurons during the brain growth spurt. Toxicol Sci 2012, 130:168-179.
21. Bittigau P., Sifringer M., Genz K., Reith E., Pospischil D., Govindarajalu S., et al. Antiepileptic drugs and apoptotic neurodegeneration in the developing brain. Proc Natl Acad Sci U S A 2002, 99:15089-15094.
22. Ikonomidou C. Triggers of apoptosis in the immature brain. Brain Dev 2009, 31:488-492.
23. Kwan P., Sills G.J., Brodie M.J. The mechanisms of action of commonly used antiepileptic drugs. Pharmacol Ther 2001, 90:21-34. [Review].
24. Béla C., Mónika B., Márton T., István K. Valproate selectively reduces EEG activity in anterior parts of the cortex in patients with idiopathic generalized epilepsy. A low resolution electromagnetic tomography (LORETA) study. Epilepsy Res 2007, 75:186-191.
25. Deckers C.L., Czuczwar S.J., Hekster Y.A., Keyser A., Kubova H., Meinardi H., et al. Selection of antiepileptic drug polytherapy based on mechanisms of action: the evidence reviewed. Epilepsia 2000, 41:1364-1374.
26. Xie X., Hagan R.M. Cellular and molecular actions of lamotrigine: possible mechanisms of efficacy in bipolar disorder. Neuropsychobiology 1998, 38:119-130.
27. Zona C., Avoli M. Lamotrigine reduces voltage-gated sodium currents in rat central neurons in culture. Epilepsia 1997, 38:522-525.
28. Miller A.A., Wheatley P., Sawyer D.A., Baxter M.G., Roth B. Pharmacological studies on lamotrigine, a novel potential antiepileptic drug: I. Anticonvulsant profile in mice and rats. Epilepsia 1986, 27:483-489.
29. Glauser T.A., Miles M.V., Tang P., Clark P., McGee K., Doose D.R. Topiramate pharmacokinetics in infants. Epilepsia 1999, 40:788-791.
30. Walton N.Y., Jaing Q., Hyun B., Treiman D.M. Lamotrigine vs. phenytoin for treatment of status epilepticus: comparison in an experimental model. Epilepsy Res 1996, 24:19-28.
31. Halonen T., Nissinen J., Pitkänen A. Effect of lamotrigine treatment on status epilepticus-induced neuronal damage and memory impairment in rat. Epilepsy Res 2001, 46:205-223.
32. Maj R., Fariello R.G., Ukmar G., Varasi M., Pevarello P., McArthur R.A., et al. PNU-151774E protects against kainate-induced status epilepticus and hippocampal lesions in the rat. Eur J Pharmacol 1998, 359:27-32.
33. Trojnar M.K., Malek R., Chroscinska M., Nowak S., Blaszczyk B., Czuczwar S.J. Neuroprotective effects of antiepileptic drugs. Pol J Pharmacol 2002, 54:557-566.
34. Gao X.M., Margolis R.L., Leeds P., Hough C., Post R.M., Chuang D.M. Carbamazepine induction of apoptosis in cultured cerebellar neurons: effects of N-methyl-d-aspartate, aurintricarboxylic acid and cycloheximide. Brain Res 1995, 703:63-71.
35. Blank N.K., Nishimura R.N., Seil F. Phenytoin neurotoxicity in developing mouse cerebellum in tissue culture. J Neurol Sci 1982, 55:91-97.
36. Czuczwar S.J., Patsalos P.N. The new generation of GABA enhancers. CNS Drugs 2001, 15:339-350.
37. Deckers C.L., Genton P., Sills G.J., Schmidt D. Current limitations of antiepileptic drug therapy: a conference review. Epilepsy Res 2003, 53:1-17.
38. Sobaniec-Lotowska M., Sobaniec W. Effect of chronic administration of sodium valproate on the morphology of the rat brain hemispheres. Neuropatol Pol 1993, 31:149-158.
39. Glier C., Dzietko M., Bittigau P., Jarosz B., Korobowicz E., Ikonomidou C. Therapeutic doses of topiramate are not toxic to the developing rat brain. Exp Neurol 2004, 187:403-409.
40. Albala B.J., Moshe S.L., Okada R. Kainic acid-induced seizures: a developmental study. Dev Brain Res 1984, 13:139-148.
41. Liu H., Kaur J., Dashtipour K., Kinyamu R., Ribak C.E., Friedman L.K. Suppression of hippocampal neurogenesis is associated with developmental stage, number of perinatal seizure episodes, and glucocorticosteroid level. Exp Neurol 2003, 184:196-213.
42. Choudhury M.A., Zaman M., Mollah A.H., Hoque M.A., Fatmi L.E., Islam M.N., et al. Iron status in children with febrile seizure. Mymensingh Med J 2013, 22:275-280.
43. Kubová H., Mares P. Anticonvulsant action of oxcarbazepine, hydroxycarbamazepine, and carbamazepine against metrazol-induced motor seizures in developing rats. Epilepsia 1993, 45:807-810.
44. Liu H., Friedman L.K., Kaur J., Keesey R. Perinatal seizures preferentially protect CA1 neurons from seizure-induced damage in prepubescent rats. Seizure 2006, 15:1-16.
45. Friedman L.K., Velísková J. GluR2 hippocampal knockdown reveals developmental regulation of epileptogenicity and neurodegeneration. Mol Brain Res 1998, 61:224-231.
46. Paxinos G., Watson C.R., Emson P.C. AChE-stained horizontal sections of the rat brain in stereotaxic coordinates. J Neurosci Methods 1980, 3:129-149.
47. Nickel B., Szelenyi I. Comparison of changes in the EEG of freely moving rats induced by enciprazine, buspirone and diazepam. Neuropharmacology 1989, 28:799-803.
48. Gallyas F., Wolff J.R., Bottcher W.H., Zaborszky L. A reliable and sensitive method to localize terminal degeneration and lysosomes in the central nervous system. Stain Technol 1980, 55:299V306.
49. Friedman L.K., Goldstein B., Rafiuddin A., Roblejo P., Friedman S. Lack of resveratrol neuroprotection in developing rats treated with kainic acid. Neuroscience 2013, 230:39-49.
50. Kaur J., Magrys B., Liu H., Friedman L.K. NR1 knockdown reduces seizure activity during a period of high seizure susceptibility. Neuromolecular Med 2007, 9:298-314.
51. Verrotti A., Scaparrotta A., Agostinelli S., Di Pillo S., Chiarelli F., Grosso S. Topiramate-induced weight loss: a review. Epilepsy Res 2011, 95:189-199. [Review].
52. Löscher W. Valproate: a reappraisal of its pharmacodynamic properties and mechanisms of action. Prog Neurobiol 1999, 58:31-59. [Review].
53. Cuadrado A., de las Cuevas I., Valdizán E.M., Armijo J.A. Synergistic interaction between valproate and lamotrigine against seizures induced by 4-aminopyridine and pentylenetetrazole in mice. Eur J Pharmacol 2002, 453:43-52.
54. Ahmad S., Fowler L.J., Whitton P.S. Effects of combined lamotrigine and valproate on basal and stimulated extracellular amino acids and monoamines in the hippocampus of freely moving rats. Naunyn Schmiedebergs Arch Pharmacol 2005, 371:1-8.
55. A receptor-mediated synaptic transmission in the basolateral amygdala: implications for its effects in seizure and affective disorders. Neuropharmacology 2002, 42:522-529.
56. Stefani A., Spadoni F., Bernardi G. Voltage-activated calcium channels: targets of antiepileptic drug therapy?. Epilepsia 1997, 38:959-965. [Review].
57. Glauser T.A. Behavioral and psychiatric adverse events associated with antiepileptic drugs commonly used in pediatric patients. J Child Neurol 2004, 19(Suppl. 1):S25-S38. [Review].
58. Lee G.M., Lee K.S., Lee E.H., Chung S. Short term outcomes of topiramate monotherapy as a first-line treatment in newly diagnosed West syndrome. Korean J Pediatr 2011, 54:380-384.
59. Brodie M.J., French J.A. Management of epilepsy in adolescents and adults. Lancet 2000, 356:323-329.
60. Perucca E. A pharmacological and clinical review on topiramate, a new antiepileptic drug. Pharmacol Res 1997, 35:241-256. [Review].
61. A receptors on principal neurons. J Pharmacol Exp Ther 2009, 330:558-566.
62. White H.S., Brown S.D., Woodhead J.H., Skeen G.A., Wolf H.H. Topiramate enhances GABA-mediated chloride flux and GABA-evoked chloride currents in murine brain neurons and increases seizure threshold. Epilepsy Res 1997, 28:167-179.
63. Rogawski M.A., Löscher W. The neurobiology of antiepileptic drugs. Nat Rev Neurosci 2004, 5(7):553-564. [Review].
64. Forcelli P.A., Kim J., Kondratyev A., Gale K. Pattern of antiepileptic drug-induced cell death in limbic regions of the neonatal rat brain. Epilepsia 2011, 52:e207-11.
65. Saghyan A, LaTorre GN, Keesey R. Sharma A, Mehta V, Rudenko V. et al. Glutamatergic and morphological alterations associated with early life seizure-induced preconditioning. Eur J Neurosci 2010;32:1897-1911.
66. Nissinen J., Large C.H., Stratton S.C., Pitkänen A. Effect of lamotrigine treatment on epileptogenesis: an experimental study in rat. Epilepsy Res 2004, 58:119-132.
67. Zhao Q., Hu Y., Holmes G.L. Effect of topiramate on cognitive function and activity level following neonatal seizures. Epilepsy Behav 2005, 6:529-536.
68. Murakami A., Furui T. Effects of the conventional anticonvulsants: phenytoin, carbamazepine, and valproic acid on sodium-potassium-adenosine triphosphatase in acute ischemic brain. Neurosurgery 1994, 34:1047-1051.
69. Pena F., Tapia R. Seizures and neurodegeneration induced by 4-aminopyridine in rat hippocampus in vivo: role of glutamate- and GABA-mediated neurotransmission and of ion channels. Neuroscience 2000, 101:547-561.
70. Smith M.D., Adams A.C., Saunders G.W., White H.S., Wilcox K.S., et al. Phenytoin- and carbamazepine-resistant spontaneous bursting in rat entorhinal cortex is blocked by retigabine in vitro. Epilepsy Res 2007, 74:97-106.
71. Cha B.H., Silveira D.C., Liu X., Hu Y., Holmes G.L. Effect of topiramate following recurrent and prolonged seizures during early development. Epilepsy Res 2002, 51:217-232.